Involvement of poly(3‐hydroxybutyrate) synthesis in catabolite repression of tetralin biodegradation genes in <i>Sphingomonas macrogolitabida</i> strain TFA

Martín-Cabello, Guadalupe; Moreno-Ruiz, Emilia; Morales, Valle; Floriano, Belén; Santero, Eduardo

doi:10.1111/j.1758-2229.2011.00273.x

Cited by 5 publications

(5 citation statements)

References 24 publications

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“…Although PHB synthesis and degradation were incorporated into iIG743, all predictions were performed without synthesis of this carbon storage granule. However, it has been reported previously that TFA cells accumulate PHB up to approximately 7% of the total biomass dry weight during growth in minimal medium plus 40 mM 3-HB 41 . As observed in Supplementary Fig.…”

Section: Discussionmentioning

confidence: 82%

Understanding the metabolism of the tetralin degrader Sphingopyxis granuli strain TFA through genome-scale metabolic modelling

García‐Romero

Nogales

Dı́az

et al. 2020

Sci Rep

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Sphingopyxis granuli strain tfA is an α-proteobacterium that belongs to the sphingomonads, a group of bacteria well-known for its degradative capabilities and oligotrophic metabolism. Strain tfA is the only bacterium in which the mineralisation of the aromatic pollutant tetralin has been completely characterized at biochemical, genetic, and regulatory levels and the first Sphingopyxis characterised as facultative anaerobe. Here we report additional metabolic features of this α-proteobacterium using metabolic modelling and the functional integration of genomic and transcriptomic data. the genomescale metabolic model (GEM) of strain TFA, which has been manually curated, includes information on 743 genes, 1114 metabolites and 1397 reactions. This represents the largest metabolic model for a member of the Sphingomonadales order thus far. the predictive potential of this model was validated against experimentally calculated growth rates on different carbon sources and under different growth conditions, including both aerobic and anaerobic metabolisms. Moreover, new carbon and nitrogen sources were predicted and experimentally validated. the constructed metabolic model was used as a platform for the incorporation of transcriptomic data, generating a more robust and accurate model. In silico flux analysis under different metabolic scenarios highlighted the key role of the glyoxylate cycle in the central metabolism of strain tfA. Members of the Sphingomonadales order, which includes the Sphingomonadaceae and Erythrobacteraceae families, are known as degraders of a large diversity of recalcitrant compounds 1. Within the Sphingomonadaceae family, the sphingomonads group, composed of the ubiquitous genera Sphingomonas, Sphingobium, Novosphingobium and Sphingopyxis 2 , contains metabolically versatile bacteria capable of using a large number of recalcitrant compounds, mainly aromatic compounds and their derivatives, as sole carbon and energy source 3. In addition, the genus Sphingopyxis includes organisms adapted to oligotrophic environments, which show specific genomic characteristics such as a low number of rRNA operons, prophages or CRISPRs sequences 4. Moreover, oligotrophs show overrepresentation of Clusters of Orthologous Groups (COGs) for lipid transport and metabolism (I) and secondary metabolite biosynthesis, transport, and catabolism (Q) among others 4 .Thus there is a need to better understand the metabolism of these degradative bacteria and to potentially reveal new insights into their degradative capabilities and lifestyle. To this end, we set out to establish a GEnome-scale metabolic Network REconstruction (GENRE) for a member of this genus that was likely to prove a powerful tool for future studies 5-8. A GENRE is a database with specific information about the species of interest generated from genomic data, and that contains detailed information about metabolism, the network of reactions, including stoichiometry and reversibility, the Gene-Protein-Reaction (GPR) associations and other available biochemical an...

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Section: Discussionmentioning

confidence: 82%

Understanding the metabolism of the tetralin degrader Sphingopyxis granuli strain TFA through genome-scale metabolic modelling

García‐Romero

Nogales

Dı́az

et al. 2020

Sci Rep

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“…However, a clear connection between CCR and the energetic status of the cell has been demonstrated in this bacterium (Figure 4). Transposon mutants affecting in phaC gene, coding for a poly(3-hydroxybutyrate) synthase, are unable to synthetize the carbon storage PHB (polyhydroxybutyrate) granule and show a partial release of thn genes CCR [56]. Conversely to what happens in the wild-type, phaC mutants prematurely induce thn genes in the presence of βHB, although maximal induction is never reached.…”

Section: Regulation Of the Thn Gene Expressionmentioning

confidence: 99%

“…The lack of SuhB or Hfq provokes a premature induction of thn genes in CCR conditions. However, only partial induction, even lower than that reached in phaC mutants, is achieved [56,57]. It has been demonstrated that suhB expression is regulated by the growth rate, being elevated at high growth rates, which would imply a high-energy status of the cells.…”

Section: Regulation Of the Thn Gene Expressionmentioning

confidence: 99%

Biodegradation of Tetralin: Genomics, Gene Function and Regulation

Floriano

Santero

Reyes‐Ramírez

2019

Genes

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Tetralin (1,2,3,4-tetrahydonaphthalene) is a recalcitrant compound that consists of an aromatic and an alicyclic ring. It is found in crude oils, produced industrially from naphthalene or anthracene, and widely used as an organic solvent. Its toxicity is due to the alteration of biological membranes by its hydrophobic character and to the formation of toxic hydroperoxides. Two unrelated bacteria, Sphingopyxis granuli strain TFA and Rhodococcus sp. strain TFB were isolated from the same niche as able to grow on tetralin as the sole source of carbon and energy. In this review, we provide an overview of current knowledge on tetralin catabolism at biochemical, genetic and regulatory levels in both strains. Although they share the same biodegradation strategy and enzymatic activities, no evidences of horizontal gene transfer between both bacteria have been found. Moreover, the regulatory elements that control the expression of the gene clusters are completely different in each strain. A special consideration is given to the complex regulation discovered in TFA since three regulatory systems, one of them involving an unprecedented communication between the catabolic pathway and the regulatory elements, act together at transcriptional and posttranscriptional levels to optimize tetralin biodegradation gene expression to the environmental conditions.

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“…Moreover, induction of thn expression by tetralin is prevented in the presence of alternative and preferential carbon sources such as β-hydroxybutyrate (βHB) or sebacic acid (Martínez-Pérez et al, 2004), but the regulatory mechanism that underlies this CCR was unknown. An extensive search for transposon mutants that expressed thn genes in CCR conditions resulted in the identification of a negative role for the polyβ-hydroxybutyrate (PHB) granule synthesis in thn gene expression (Martín-Cabello et al, 2011). Mutants lacking the PHB synthase PhaC showed partial de-repression of thn expression in CCR conditions due to the absence of the polymer, which seems to be sensed as a signal for carbon sufficiency.…”

Section: Introductionmentioning

confidence: 99%

SuhB, a small non‐coding RNA involved in catabolite repression of tetralin degradation genes in Sphingopyxis granuli strain TFA

García‐Romero

Förstner

Santero

et al. 2018

Environmental Microbiology

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Global dRNA-seq analysis of transcription start sites combined with in silico annotation using Infernal software revealed the expression of 91 putative non-coding sRNA in Sphingopyxis granuli TFA cells grown on different carbon sources. Excluding housekeeping sRNAs, only one additional sRNA, which belongs to the Rfam SuhB family (RF00519), was detected by Infernal but with an incorrect size according to the experimental results. SuhB is highly conserved across the Sphingopyxis genus. Expression data revealed that SuhB is present in rapidly growing TFA cells. A suhB deletion mutant exhibited de-repression of tetralin degradation (thn) gene expression and higher amounts of their LysR-type activator, ThnR, under conditions of carbon catabolite repression (CCR). Interaction between SuhB and the 5'UTR of thnR mRNA was demonstrated in vitro. Moreover, co-immunoprecipitation experiments, combined with fluorescence measurements of gfp fusions to the 5'UTR of thnR mRNA and the phenotype of an hfq deletion mutant, suggest the involvement of Hfq in this interaction. Taken together, these data support an Hfq-mediated repressive role for SuhB, on ThnR mRNA translation that prevents thn gene induction. SuhB, which is a highly conserved sRNA in the Sphingopyxis genus, is the first identified element directly involved in CCR of thn gene expression in S. granuli strain TFA.

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Involvement of poly(3‐hydroxybutyrate) synthesis in catabolite repression of tetralin biodegradation genes in Sphingomonas macrogolitabida strain TFA

Cited by 5 publications

References 24 publications

Understanding the metabolism of the tetralin degrader Sphingopyxis granuli strain TFA through genome-scale metabolic modelling

Understanding the metabolism of the tetralin degrader Sphingopyxis granuli strain TFA through genome-scale metabolic modelling

Biodegradation of Tetralin: Genomics, Gene Function and Regulation

SuhB, a small non‐coding RNA involved in catabolite repression of tetralin degradation genes in Sphingopyxis granuli strain TFA

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